Male Gonads in Armadillidium vulgare

The Carcinological Society of Japan

NII-Electronic Library Service

The CarcinologicalSociety of Japan

CRUSTACEAN RESEARCH, NO. 24: 93-103, 1995

Morphological studies on sexual differentiation inArmadillidium vuigare (Isopoda: Armadillidae):androgenic gland and male sexual characters

Sachiko Suzuki and Keaji Yamasaki

Abstract - The process of sexual dif-ferentiation of the isopod, Armadil-lidium vuigare was studied morphologi-

cally during early stages of post-embry-onic development. Sexual diflrerentiationof gonads was first observed in the testesat the fourth stage. Male endopodites,

which develop later into male copulatory

orgaris as one of secondary sexual char-

acters, started to elongate at the fifthstage. The androgenic glands were ob-

served morphologically at the sixth

stage. This study suggests that the go-nadal primordia start to differentiateinto tegtes in the absenee of visible an-drogenic glands in male A. vuigare. Thedevelopmental process of male internal

and external sexual characters in mala-

costracan Crustacea were discussed.

Introduction

Sexual diffbrentiation among malacos-

tracan Crustacea has been studied chiefly

in amphipods (Charniaux-Cotton, 1954,1959, 1960, 1962; Veillet & Graf, 1958;Charniaux-Cotton & Ginsburger-Vogel,1962; Hort-Legrand et al., 1973, 1974), inisopods (Takewaki & Nakamura, 1944;Katakura, 1961, 1967, 1984; Juchault &Legrand, 1964; Reidenbach, 1971;Berreur-Bonnenfant & Inagaki, 1973;Juchault, 1977; Lane, 1977; Hasegawa &Katakura, 1981, Katakura & Hasegawa,1983; Suzuki et al., 1990; Suzuki &Yamasaki, 1991a, 1991b) and in decapods(Hoffman, 1969; Payen, 1973, 1974; LeRoux, 1976; Nagamine et al,, 1980a,

1980b; Nagamine & Knight, 1980, 1987;Sagi et al., 1990; Lee et at., 1993, 1994).There are also recent reviews (Char-niaux-Cotton & Payen, 1985, 1988 ;Payen 1986, 1991; Katakura, 1989;Chaniaux-Cotton et al., 1992; Hasegawaet al., 1993) dealing with sexual difft)ren-tiation in Crustacea. The data are consis-

tent with the hypothesis that the andro-

genic glands (AG) control diffbrentiationof all the male sexual characters throughthe secretion of the androgenic gland hor-mone (AGH). In the researches of the iso-pod A vuigare, the AGH was shown as a

peptide hormone from male reproductive

organs (Hasegawa et al., 1987; Martin et

al., 1990; Hasegawa et al., 1993). Recentlythat peptide has been reported as a novel

peptide in seminal vesicle and vas defer-ens (Nagasawa et al., 1994). That is tosay, the AGH has not yet been isolated inCrustacea. However, this male horrnonehas been thought to determine the devel-opment and difft)rentiation ofthe gonadalsex and phenotypic sex ofmale Crustacea.On the other hand, in genetic femalesAGs do not develop and the gonadal pri-mordia develop into ovaries spontane-

ously. Crustacean sexual differentiation,therefore, depends on the presence or ab-

sence of AGs. This hypothesis is appli-

cable to the hormonal control of sexual

difft}rentiatien ofA. vuigare because sex

reversal has been observed in experimen-tal animals bearing (Katakura, 1967;Hasegawa & Katakura, 1983) or not bear-ing (Suzuki & Yamasaki, 1991a) AGs.The sex-reversal experiments done with




94 S. SUZUKI & K, YAMASAKI

Fig. 1. The copulatory

Armodillidiunt vuigare,

Normal Male Ovariectomized Female

organs ef a normal mature male and an ovariectomized

The females were ovariectomized at an immature stage,

female

this species also show clearly that the go-nadal primordia of both sexes have a com-

mon origin and sexual bipotentiality.

The endopodites ofthe first abdominal

legs of young male A vuigare begin to

elongate at the fburth post-embryonicmolt and develop through successiye

melts, progressively acquiring the mor-

phology of copulatery organs (Katakura,1961; Hasegawa & Katakura, 1985;Suzuki et al., 1990) which are one of thesecondary male characters. In this spe-cies, implantation of AGs into immaturefemales induces masculinization of the

endopodites, and after several molts these

females form copulatory organs whose ap-

pearance is the same as that of the en-

dopodites of mature males (Katakura &

Hasegawa, 1983; Hasegawa & Katakura,

1985). Also, elongation of the endopodites

was often observed with females whose

gonads had been removed while the indi-

viduals were still sexually immature.

However, elongation of their endopodites

stopped at a low developmental level afterseveral molts fo11owing ovariectomy

(Suzuki & Yamasaki, 1994) as shown in

Figure 1. Furthermore, vitellogenin could

be detected in their hemolymph (Suzuki,1987; Suzuki et al., 1990). These observa-

tions suggest that AGs were either not

present or if present, were not functionalin these ovariectomized females. How-ever, questions remain as to what caused

this endopodite elongation in the ovari-

ectomized females.

The purpose of our present study was

to obtain fundamental knowledge of the

process of sexual differentiation in maleA. vuigare. Post-embryonic developmentof internal and external reproductive or-

gans of males was investigated morpho-logically from the sexually undiffbrenti-

ated stage until the sexually mature

stage. In addition, the relationship of de-

velopmental timing between formation of

AGs and sexual differentiation of male

characters was also examined.




SEXUAL DIFFERENTIAMVION IN CRUSTACEA 95

Materials and Methods

Animals Specimens of egg-bearing female A.vuigare were collected and reared in thelaboratory at 25±20C as described previ-ously (Suzuki, 1987). After hatching,

young of this species remain in the mar-

supium of their mother for several days.To study sexual difTerentiation of post-embryonic developments, specimens of

the young were obtained the day ofreleas-

ing from the marsupium. The number of

molts after hatching was used to definethe stages of post-embryonic develop-ment. First stage young underwent theirfirst ecdysis synchronously soon after

they were released from the marsupium.

That is, they were in the second stage of

post-embryonic development within 24hours of releasing. Until the fourth stage,sexual dimorphism of the external char-

acters is hardly detectable (Katakura,1984). At the fifth stage, a male can bedistinguished from a female for the firsttime because of elongation of the en-

dopodites of the first abdominal legs(Katakura, 1984; Suzuki et al., 1990).This character is used in the later stagesto determine the gender of this species. Toobtain third and fourth stage males, we

caused sex reversal of genetic males intofemales by partial gonadeetomy (Suzuki& Yamasaki, 1991a). T[he sex-reversed fe-males of genetic males were bred with

normal males and produced only male off-

spring which were used after rearing fortwo or three weeks fo11owing releasing.

Develqpment of internal and external re-

productive organs in males

Sexual differentiation of intemal and

external characters was looked for mor-phologically after each molt. Third toeighth stage males were dissected in crus-tacean physiological saline (Suzuki et al.,

1990) with the aid of fine forceps under a

dissecting microscope. Fresh internal re-

productive organs were observed in saline

with a compound microscope. Morphologi-cal differentiation of copulatory organs

was observed under a dissecting micro-

scope. Measurement of structures wag

made with the aid of an ocular microme-

ter in a light microscope or a caliper under

a dissecting microscope.

71ransplantation of male reproductive or-

gans into females The internal reproductive organs were

surgically obtained from males in thethird to eighth developmental stages.

Males were dissected in saline (40C). Apair of organs were immediately trans-

planted into the recipients which were

immature eighth stage females (5.2 mmin body length). Because of the large size

of reproductive organs from the eighth

stage males only the left or right halfwasimplanted. Implantation was perfbrmedthrough a slit between the fourth and

fifth thoracic segments ofthe eighth stage

females, as described previously (Suzuki& Yamasaki, 1991a). After implantation,whether masculinization of females oc-

curred was determined by looking for theelongation of the endopodites at every

molt. In the masculinized females, the

morphological structure and size of the

copulatory organs were determined and

compared with those of normal mature

males (more than 6.0 mm in body length)after the fifth post-operative molt

(Katakura, 1984).

Results

Morpholngical dij7Terentiation of internalreproductive organs in males

By tlie end ofthe second week ofpost-

embryonic development fo11owing releas-ing from the marsupium, the young were

in the third stage, averaging 2,O mm inbody length. Sexual dimorphism of the

gonadal primordia among the geneticmales (Figs. 2-A and 3) and the animals

whose gender was unknown but which

were used as a complementing female




96 S. SUZUKI & K YAMASAKI

specimens was not yet apparent in this

stage (Flg. 3), At the anterior portion of

their gonadal primordia several thinstrands of cells were visible (Fig. 2-A).Morphological diffbrentiation of the go-nads into ovaries or testes was observed

at the fburth stage (Fig. 3). In fburth stage

animals, 2.4 mm in body length, sexual

differentiation of the male gonadal pri-mordia was obvious by the end of thethird week of post-embryonie develop-ment. The testicular primordia on bothsides of the body elongated anteriorly and

increased in size, T-1 starting earlier thanT-2 (Fig. 2-B). In the fifth stage (2.9 mmin body length), the testicular primor-dium T-3 (Fig. 2-C) appeared by the end of

the fourth week of post-embryonic devel-opment. However, AGs were not presentat this stage. Early in sixth stage (3.5mm), a pair of AGs-1 were visible at theend of each T-1 testis (Fig. 2-D) and two

additional pairs of AGs then appeared in

the fo11owing order, AG-2 and AG-3 in two

or three day interval in the fifth or sixth

week (Fig. 4). These AGs are located at

the cephalic end of each testis in A

vuigare. The testes ofseventh stage males

(4.4 mm) were fiIled with mature sperms

in the seventh or eighth week ofpost-em-

bryonic development (Fig. 2-E). Duringthe eighth stage (5.2 mm), sperm moved

from the testes into the seminal vesicles

and then into the vasa deferentia (Figs. 2-

F and 3). The total period of male develop-

mental growth from the first to the eighth

stage was about 10 weeks after releasing

from the marsupium.

For comparison with males, gonadaldevelopment of females was also ob-

served. The internal reproductive organs

of the females were morphologically sim-

pler than those of males. The developingovaries increased in size gradually with

no remarkable change in structure duringthe third to the eighth stage of post em-

bryonic development, as shown in Fig. 3.

Rormation ofcopulatorrv organs in males

Sexual differentiation of male copula-

tory organs first occurs in the fifth stagewhen a slight elongation of the en-

dopodites occurs (Fig. 4). The endopodites

of males rapidly increased in size and

complexity at subsequent molts. The

copulatory organs of eighth stage males

were identical to those of mature males.

Ef7iect of transplantation of male gonadsinto immat"re females The AGs first appeared in sixth stage

males (Figs. 2 and 3). Gonad transplanta-

tion was carried out to determine whether

the cells ofAGs had already differenti ated

in the gonadal primordia of youngermales without forming distinct AGs.

Eighth stage females were implanted

with either a pair or only one of the repro-

ductive organs from third to eighth stage

males, After the first post-operative molt,

masculinization of endopodites was ob-

served in more than 50% of the femalesimplanted with gonads from sixth toeighth stage males (Fig. 5). The en-

dopodites of these masculinized females

continued to elongate in subsequent molts

and eventually acquired the form of male

copulatory organs after five post-opera-tive molts. We observed no structural difference between the copulatory organs of

maseulinized females and normal mature

males. On the other hand, all but one of

the females which were implanted with

gonadal primordia from third to fifthstage males did not become masculinized

after the first post-operative molt and didnot form copulatory organs in subsequent

molts. One female of the 23 which were

implanted with gonads from fifth stagemales developed normal male copulatory

organs (Fig. 5), which suggests that AGsmight have already diffbrentiated in a

small proportion of males during the fifth

stage.

The results of the transplantation ex-

periments (Fig. 5) are consistent with the

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SEXUAL DIFFERENTIATION IN CRUSTACEA 97

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Fig. 2, Development of male gonads in Armadillidiunz vulgare. Photomierographs show freshmale gonads from the third to eighth stages of post-embryenic development, A, third stage; B,fourth stage; C, fifth stage; D, sixth stage; E, seventh stage; F, eighth stage. T, testis; Ag, andro-

genic gland; Od, oviduct; Sv, seminal vesicle; Vd, vas deferens. Scalebars = 200 pm. The numbers

ofT or Ag (T-1, Ag-1 etc.) show the order ofdifferentiating time.

morphological observations of gonadal de-velopment (Figs. 2 and 3); that is, AGswere clearly seen in sixth stage male A.vuigare.

Discussion

Process of sexual difilerentiation inArinadillidium vuigare

male

The results presented herein reveal

that the first morphological evidence of

sexual difft)rentiation is the formation of

testes in fburth stage males and that AGsare first seen in sixth stage ofpost-embry-

onie development. The results also sug-

gest that sexual diffbrentiation of male

gonadal primordia may start in the third

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98 S, SUZUKI & K. YAMASAKI

oa

i/8

rs3 Stage

T

T

14

I.

T

15

oooo

l. 6

oo

ooo

l. 7

oo

oe

oZoeoo

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ov

Fig. 3. Gonadal development in normal male and femaleArmadillidiurn vuigare. Schematic rep-resentation ofthe sexual dimorphism ofthe internal reproductive organs from the third to eighthstages of post-embryonic development. T, testis; Ag, androgenic gland; Sv, seminal vesicle; Vd,vas deferens; Od, oviduct; Ov, ovary. Scale bars = 200 ym.

stage, during an undifft)rentiated periodof the AGs. Testicular primordia are pre-sumably induced to diffbrentiate in the

third stage by sex-differentiating factors.Furthermore, male copulatory organs,

which are ene of the secondary eharacters

in males, also start their differentiation inthe fifth stage, prior to the formation ofthe AGs. It appears, therefore, that theremay be at least one factor capable of

stimulating development of endopodites

in fourth stage males ofthis species. It ispossible that this factor may be able to

produce elongation of the endopodites inthe ovariectomized young females which

have been mentioned in the introduction

(Fig, 1). Once AGs are fbrmed at the sixth

stage, AGH appears to control the subse-

quent sexual diffbrentiation in males as

shown by experimental reversal of sex inthis species (Katakura, 1967; Hasegawa& Katakura, 1983; Suzuki & Yamasaki,1991a).

The timing of sexual differentiation inA. vuLgare was examined previously by

Lane (1977) who reported the onset of

sexual differentiation in the second and

third weeks of post-embryonic develop-ment, which is in agreement with our

present results.





oD

3 Stage o

T-1

T-2

14

I

T-S

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15

I

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. 6

1. 7

g-5

T-3

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cpvc)

I

( I]llr[ l) NI

En I l

Ex

En

Fig. 4, Development of male gonads and copulatory organs inArmadiltidium vuigare. Schematicrepresentation ofthe differentiation ofmale sexual characters from the third te eighth stages ofdevelopmental growth. T, testis; Ag, androgenic gland; Sv, seminal vesicle; Vd, vas deferens; Od,oviduct; En, endopodite; Ex, exopedite. Scale bars = 200 pm. The numbers of T or Ag (T-1, Ag-1etc.) show the order ofdiffbrentiating time.

Sexual difll3rentiation in malacostracan

Crustacea

The current dogma concerning hor-monal regulation of sexual differentiationin Crustacea was first proposed on thebasis of studies with an amphipod

(Charniaux-Cetton & Payen, 1985). Ac-cording to the hypothesis, male sex-deter-

mining genes control the development of

the AGs and female sex-determining

genes are responsible for inhibiting differ-entiation to a functional state of the AGsin females. In genetic males, the AGs se-

crete AGH, and the hormone causes de-velopment ofthe male gonads and second-

ary sexual characters. Katakura (1989)has also presented a similar hypothesison endocrine and genetic controls of

sexual differentiation in the isopod, A.vuigare, and proposed that sexual devel-

opment begins when the primordial AG-cells of genetic males first appears, priorto development of the primary and sec-

ondary sexual characters.

On the other hand, in some decapodsthere are several ebservations which indi-cate that male diffbrentiation begins be-fore the AGs become visible (Payen, 1973,1974; Le Roux, 1976; Charniaux-Cotton &Payen, 1985; Lee et al., 1994). These ob-

servations may be not consistent with

the current hypothesis. Furthermore, inmales of the isopod Ligia italica the ap-

pendix masuculina has also reported to berecognizable when the gonads begin todevelop in an undifferentiated sexual

stage (Berreur-Bonnenfant & Inagaki,1973). Our present results obtained with

the isopod A. vuigare are similar to theobservations with decapods and the iso-

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lmmature Female

(Recipient)

.

Masculinized

Femate

co

gehlXE9obeg=aoo.+.-o-

c oE

a o m > oa

100

50

3 4 5 6

Stages of Male

7

(Donor)8

5. Development of copulatory organs in females after implantation of male gonads. MaleFig.gonads were surgically obtained from third to eighth stage males (donors) and transplanted into

. Development of the copula-immature eighth stage females (recipients) (5.2 mm in body length)tery organs was followed for five post-operative molts after implantation ofthe male gonads. The

number at each point in the graph represents the number of females implanted. Co, copulatory

organs.

pod, L. italica.

In male decapods, endocrine cells have

been postulated to secrete AGH befbre theAGs differentiate, in the gonadal primor-dia or elsewhere (Nagamine et al,, 1980a;

Charniaux-Cotton & Payen, 1988; Lee et

al., 1994). In the isopod A. vuigare, it has

also reported that the differentiation of

the AGs is independent of that of the go-nads (Lane, 1977). However, we could

make andrectomized animals surgically

by eomplete gonadectomy or partial

gonadectomy using fifth stage males,

whose AGs being not yet visible in thisspecies (Suzuki et al., 1990; Suzuki &Yamasaki, 1991a). Our experiments were

based on the supposition that AGs have a

developmental origin in gonadal primor-dium. But it is now unclear whether there

are already AG cells elsewhere whieh can

secrete AGH befbre the morphological ob-

servation of the AGs in A. vuigare.

Until now there has been no evidence

that male sex-determining genes act di-





rectly upon the development of the AGs.Investigation at the molecular level isneeded to determine strictly whether sex-

determining genes can induce AG diffbr-entiation prior to the differentiation of the

gonadal primordium during the sexually

undifferentiated stage.

Acknowledgments

We thank Professors TadakazuOhoka, Shiro Tomino (Tokyo Metropoli-tan University), Yasutoshi Katakura

(Sohka University) and Masahide Yoshi-da (Kanagawa Prefectural College) fbrtheir advice and comments during thecourse of this investigation. We also wish

to express our gratitude to ProfessorMilton Fingerman (Tulane University)for his help in reviewing the manuscript.

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(SS) Biological Laboratory, Kanagawa Pre-fectural College, Yokohama 241, Japan; (KY)Department of Biology, Tokyo MetropolitanUniversity, Hachiollji, Tokyo 192-03, Japan.

Male Gonads in Armadillidium vulgare

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